Biodiversity cradles and museums segregating within hotspots of endemism

Abstract

The immense concentrations of vertebrate species in tropical mountains remain a prominent but unexplained pattern in biogeography. A long-standing hypothesis suggests that montane biodiversity hotspots result from endemic species aggregating within ecologically stable localities. Here, the persistence of ancient lineages coincides with frequent speciation events, making such areas both 'cradles' (where new species arise) and 'museums' (where old species survive). Although this hypothesis refers to processes operating at the scale of valleys, it remains supported primarily by patterns generated from coarse-scale distribution data. Using high-resolution occurrence and phylogenetic data on Andean hummingbirds, we find that old and young endemic species are not spatially aggregated. The young endemic species tend to have non-overlapping distributions scattered along the Andean treeline, a long and narrow habitat where populations easily become fragmented. By contrast, the old endemic species have more aggregated distributions, but mainly within pockets of cloud forests at lower elevations than the young endemic species. These findings contradict the premise that biogeographical cradles and museums should overlap in valley systems where pockets of stable climate persist through periods of climate change. Instead, Andean biodiversity hotspots may derive from large-scale fluctuating climate complexity in conjunction with local-scale variability in available area and habitat connectivity.

Keywords: Andes; biodiversity; hummingbirds; maintenance; range size; speciation.

Figure 1.

Regional richness pattern of young and old endemic species. (a) The richness of endemic hummingbirds is defined as the 25% fraction of species in the north and central Andes (grey shade; [32]) with the smallest geographical ranges. (b) The richness of young endemic species, i.e. the 25% fraction of endemic hummingbirds with the shortest terminal branch lengths. (c) The richness of old endemic species, i.e. the 25% fraction of endemic hummingbirds with the longest terminal branch lengths. The pie diagrams show the differences in the species' habitat preferences. The inner circles represent the frequency distribution of hummingbird species occurring in one or several habitats. The outer diagram shows the fractions of hummingbirds that are restricted to one single habitat. (Online version in colour.)

Figure 2.

Disjunct distributions of young and old endemic species. Colours highlight grid cells with more young or old endemic species than expected from a biogeographical null model. The grey-shaded area marks the central and northern Andes [32], constituting the biogeographical source pool. The paintings (by Jon Fjeldså) show representatives of young and old endemic species from different regions in the Andes. (Online version in colour.)

Figure 3.

Richness-frequency distribution of young and old endemic species. The plot comprises the subset of grid cells with a standardized richness of young or old endemic species exceeding 0.5 (highlighted in black on the map). The threshold of 0.5 indicates that grid cells contain more of either age class than sampled by the majority of null model iterations. (Online version in colour.)

Figure 4.

Segregations in elevations between young and old endemic species. (a) The richness of young endemic species peaks at higher elevations than old endemic species. Adding missing species to the phylogeny caused slight uncertainty in the composition of young and old endemic species (electronic supplementary material, table S10e). This uncertainty produces the figure's 95% confidence intervals (shaded areas). (b) Elevational variation in terminal branch lengths in million years (Myr). Here, missing species were added to the phylogeny using the median branch length for 1000 phylogenetic trees (electronic supplementary material, table S10a). The dashed lines represent the quartile boundaries used for selecting young (blue) and old (red) endemic species. (Online version in colour.)

Figure 5.

Hypothesized scale-dependency of speciation and extinction processes within a tropical mountain system, represented by the east Andean Cordillera (illustration by Jon Fjeldså). The grey bars' thickness indicates the levels of the factors, processes and patterns at different elevational zones. At the regional–continental scale of extent (a), historical climate dynamics in conjunction with topographic complexity (termed ‘fluctuating climatic complexity’; [19]) promotes speciation and lowers extinction rates. The result is young and old endemic species aggregating in tropical mountains [9,10,19]. At the scale of valleys within mountains (b), surface area and habitat connectivity become more important determinants of the speciation and extinction processes. The narrow treeline zone with patchy vegetation promotes speciation at high altitudes, resulting in a scattered distribution of young endemic species [13,14]. Above the treeline ecotone, the surface area and habitat connectivity increase if the highlands reach a plateau. The habitats' width and connectivity increase towards the cloud forest at mid-elevation, providing more optimal conditions (i.e. low extinction) for the persistence of old endemic species. (Online version in colour.)